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Journal of Environmental Science and Health, Part B
Pesticides, Food Contaminants, and Agricultural Wastes
Volume 57, 2022 - Issue 9
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Research Article

The integrated biomarker response in three anuran species larvae at sublethal concentrations of cypermethrin, chlorpyrifos, glyphosate, and glufosinate-ammonium

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References

  • Dudgeon, D.; Arthington, A. H.; Gessner, M. O.; Kawabata, Z. I.; Knowler, D. J.; Lévêque, C.; Naiman, R. J.; Prieur-Richard, A. H.; Soto, D.; Stiassny, M. L. J.; Sullivan, C. A. Freshwater Biodiversity: Importance, Threats, Status and Conservation Challenges. Biol. Rev. Camb. Philos. Soc. 2006, 81, 163–182. DOI: 10.1017/S1464793105006950.
  • Sparling, D.; Fellers, G. Comparative Toxicity of Chlorpyrifos, Diazinon, Malathion and Their Oxon Derivatives to Larval Rana boylii. Environ. Pollut. 2007, 147, 535–539. DOI: 10.1016/j.envpol.2006.10.036.
  • Relyea, R. A Cocktail of Contaminants: How Mixtures of Pesticides at Low Concentrations Affect Aquatic Communities. Oecologia 2009, 159, 363–376. DOI: 10.1007/s00442-008-1213-9.
  • Robles-Mendoza, C.; Zúñiga-Lagunes, S. R.; Ponce de León-Hill, C. A.; Hernández-Soto, J.; Vanegas-Pérez, C. Esterases Activity in the Axolotl Ambystoma mexicanum Exposed to Chlorpyrifos and Its Implication to Motor Activity. Aquat. Toxicol. 2011, 105, 728–734.
  • Peltzer, P. M.; Junges, C. M.; Attademo, A. M.; Bassó, A.; Grenón, P.; Lajmanovich, R. C. Cholinesterase Activities and Behavioural Changes in Hypsiboas pulchellus (Anura: Hylidae) Tadpoles Exposed to Glufosinate Ammonium Herbicide. Ecotoxicology 2013, 22, 1165–1173. DOI: 10.1007/s10646-013-1103-8.
  • Connon, R. E.; Geist, J.; Werner, I. Effect-Based Tools for Monitoring and Predicting the Ecotoxicological Effects of Chemicals in the Aquatic Environment. Sensors 2012, 12, 12741–12771. DOI: 10.3390/s120912741.
  • Rohr, J. R.; Salice, C. J.; Nisbet, R. M. The Pros and Cons of Ecological Risk Assessment Based on Data from Different Levels of Biological Organization. Crit. Rev. Toxicol. 2016, 46, 756–784.
  • Devin, S.; Burgeot, T.; Giambérini, L.; Minguez, L.; Pain-Devin, S. The Integrated Biomarker Response Revisited: Optimization to Avoid Misuse. Environ. Sci. Pollut. Res. Int. 2014, 21, 2448–2454.
  • Darvesh, S.; Hopkins, D. A.; Geula, C. Neurobiology of Butyrylcholinesterase. Nat. Rev. Neurosci. 2003, 4, 131–138.
  • Peterson, E. K.; Buchwalter, D. B.; Kerby, J. L.; Lefauve, M. K.; Varian-Ramos, C. W.; Swaddle, J. P. Integrative Behavioural Ecotoxicology: Bringing Together Fields to Establish New Insight to Behavioural Ecology, Toxicology, and Conservation. Curr. Zool. 2017, 63, 185–194. DOI: 10.1093/cz/zox010.
  • Widder, P. D.; Bidwell, J. R. Tadpole Size, Cholinesterase Activity, and Swim Speed in Four Frog Species after Exposure to Sub-Lethal Concentrations of Chlorpyrifos. Aquat. Toxicol. 2008, 88, 9–18. DOI: 10.1016/j.aquatox.2008.02.008.
  • Denoël, M.; D'Hooghe, B.; Ficetola, G. F.; Brasseur, C.; De Pauw, E.; Thomé, J. P.; Kestemont, P. Using Sets of Behavioural Biomarkers to Assess Short-Term Effects of Pesticide: A Study Case with Endosulfan on Frog Tadpoles. Ecotoxicology 2012, 21, 1240–1250. DOI: 10.1007/s10646-012-0878-3.
  • Juszczak, G. R.; Lisowski, P.; Sliwa, A. T.; Swiergiel, A. H. Computer Assisted Video Analysis of Swimming Performance in a Forced Swim Test: Simultaneous Assessment of Duration of Immobility and Swimming Style in Mice Selected for High and Low Swim-Stress Induced Analgesia. Physiol. Behav. 2008, 95, 400–407. DOI: 10.1016/j.physbeh.2008.07.003.
  • Tooming, E.; Merivee, E.; Must, A.; Sibul, I.; Williams, I. Sub-Lethal Effects of the Neurotoxic Pyrethroid Insecticide Fastac® 50EC on the General Motor and Locomotor Activities of the Non-Targeted Beneficial Carabid Beetle Platynus assimilis (Coleoptera: Carabidae). Pest. Manag. Sci. 2014, 70, 959–966. DOI: 10.1002/ps.3636.
  • Egea-Serrano, A.; Tejedo, M. Contrasting Effects of Nitrogenous Pollution on Fitness and Swimming Performance of Iberian Waterfrog, Pelophylax perezi (Seoane, 1885), Larvae in Mesocosms and Field Enclosures. Aquat. Toxicol. 2014, 146, 144–153. DOI: 10.1016/j.aquatox.2013.11.003.
  • Sharma, A.; Kumar, V.; Shahzad, B.; Tanveer, M.; Sidhu, G. P. S.; Handa, N.; Kohli, S. K.; Yadav, P.; Bali, A. S.; Parihar, R. D.; et al. Worldwide Pesticide Usage and Its Impacts on Ecosystem. SN Appl. Sci. 2019, 1, 1–16. DOI: 10.1007/s42452-019-1485-1.
  • Phillips, M. W. A. Agrochemical Industry Development, Trends in R&D and the Impact of Regulation. Pest Manag. Sci. 2020, 76, 3348–3356. DOI: 10.1002/ps.5728.
  • Grube, A.; Donaldson, D.; Kiely, T.; Wu, L. Pesticide's Industry Sales and Usage 2006 and 2007 Market Estimates. United States Environmental Protection Agency, Office of Pesticide Programs. Biological and Economic Analysis Division: Washington, DC. Report No. EPA 733-R-11-001, 2011; pp 1–41.
  • Wagner, N.; Reichenbecher, W.; Teichmann, H.; Tappeser, B.; Lötters, S. Questions Concerning the Potential Impact of Glyphosate-Based Herbicides on Amphibians. Environ. Toxicol. Chem. 2013, 32, 1688–1700. DOI: 10.1002/etc.2268.
  • Greulich, K.; Pflugmacher, S. Differences in Susceptibility of Various Life Stages of Amphibians to Pesticide Exposure. Aquat. Toxicol. 2003, 65, 329–336.
  • Manjunatha, B.; Philip, G. H. Reproductive Toxicity of Chlorpyrifos Tested in Zebrafish (Daniorerio): Histological and Hormonal End Points. Toxicol. Ind. Health 2016, 32, 1808–1816. DOI: 10.1177/0748233715589445.
  • Lajmanovich, R. C.; Peltzer, P. M.; Junges, C. M.; Attademo, A. M.; Sanchez, L. C.; Bassó, A. Activity Levels of B-Esterases in the Tadpoles of 11 Species of Frogs in the Middle Paraná River Flood Plain: Implication for Ecological Risk Assessment of Soybean Crops. Ecotoxicol. Environ. Saf. 2010, 73, 1517–1524. DOI: 10.1016/j.ecoenv.2010.07.047.
  • Attademo, A. M.; Peltzer, P. M.; Lajmanovich, R. C.; Cabagna Zenklusen, M.; Junges, C. M.; Bassó, A. Biological Endpoints, Enzyme Activities, and Blood Cell Parameters in Two Anuran Tadpole Species in Rice Agroecosystems of Mid-Eastern Argentina. Environ. Monit. Assess. 2014, 186, 635–649. DOI: 10.1007/s10661-013-3404-z.
  • IUCN: The International Union for Conservation of Nature and Natural Resources. An Analysis of Amphibians on the 2010. IUCN Red List, 2010. www.iucnredlist.org/amphibians.
  • Vaira, M.; Akmentins, M.; Attademo, A.; Baldo, D.; Barrasso, D.; Barrionuevo, S.; Basso, N.; Blotto, B.; Cairo, S.; Cajade, R.; et al. Categorización Del Estado de Conservación de Los Anfibios de la República Argentina. Cuadernos de Herpetología 2012, 26, 131–159.
  • Attademo, A. M.; Peltzer, P. M.; Lajmanovich, R. C. Amphibians Occurring in Soybean and Implications for Biological Control in Argentina. Agric. Ecosyst. Environ. 2005, 106, 389–394. DOI: 10.1016/j.agee.2004.08.012.
  • Peltzer, P. M.; Lajmanovich, R. C.; Attademo, A. M.; Beltzer, A. H. Diversity of Anurans across Agricultural Ponds in Argentina. Biodivers. Conserv. 2006, 15, 3499–3513. DOI: 10.1007/s10531-004-2940-9.
  • Duré, M. I.; Kehr, A. I.; Schaefer, E. F.; Marangoni, F. Diversity of Amphibians in Rice Fields from North-Eastern Argentina. Interciencia 2008, 33, 523–527.
  • Gosner, K. L. A Simplified Table for Staging Anuran Embryos and Larvae with Notes on Identification. Herpetologica 1960, 16, 183–190.
  • ASIH, HL, SSAR. Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research, Herpetological Animal Care and Use Committee (HACC) of the American Society of Ichthyologists and Herpetologists. ASIH: Washington, DC, 2011.
  • Kingbley, G. The Direct Biuret Method for the Determination of Serum Proteins as Applied to Photoelectric and Visual Colorimetry. J. Lab. Clin. Med. 1942, 27, 840–845.
  • Ellman, G. L.; Courtney, K. D.; Andres, V.; Jr.; Featherstone, R. M. A New and Rapid Calorimetric Determination of Cholinesterase Activity. Biochem. Pharmacol. 1961, 7, 88–95. DOI: 10.1016/0006-2952(61)90145-9.
  • Beliaeff, B.; Burgeot, T. Integrated Biomarker Response: A Useful Tool for Ecological Risk Assessment. Environ. Toxicol. Chem. 2002, 21, 1316–1322.
  • RStudio Team. RStudio: Integrated Development for R. RStudio, Inc.: Boston, MA, 2016. http://www.rstudio.com/.
  • Scott, G.; Sloman, K. The Effects of Environmental Pollutants on Complex Fish Behaviour: integrating Behavioural and Physiological Indicators of Toxicity. Aquat. Toxicol. 2004, 68, 369–392.
  • Junges, C. M.; Lajmanovich, R. C.; Peltzer, P. M.; Attademo, A. M.; Bassó, A. Predator-Prey Interactions between Synbranchus marmoratus (Teleostei: Synbranchidae) and Hypsiboas pulchellus Tadpoles (Amphibia: Hylidae): Importance of Lateral Line in Nocturnal Predation and Effects of Fenitrothion Exposure. Chemosphere 2010, 81, 1233–1238. DOI: 10.1016/j.chemosphere.2010.09.035.
  • Polat, H.; Erkoç, F. Ü.; Viran, R.; Koçak, O. Investigation of Acute Toxicity of Beta-Cypermethrin on Guppies Poecilia Reticulata. Chemosphere 2002, 49, 39–44.
  • Quaranta, A.; Bellantuono, V.; Cassano, G.; Lippe, C. Why Amphibians Are More Sensitive than Mammals to Xenobiotics. PLoS One 2009, 4, e7699. DOI: 10.1371/journal.pone.0007699.
  • Berrill, M.; Bertram, S.; Wilson, A.; Louis, S.; Brigham, D.; Stromberg, C. Lethal and Sublethal Impacts of Pyrethroid Insecticides on Amphibian Embryos and Tadpoles. Environ. Toxicol. Chem. 1993, 12, 525–539. DOI: 10.1002/etc.5620120313.
  • Majumder, R.; Kaviraj, A. Variation in Acute Toxicity between Technical Grade and Commercial Formulation of Cypermethrin to Some Non-Target Freshwater Organisms. Int. J. Curr. Res. 2015, 7, 1675516755–1675516759.
  • Curi, L. M.; Boccioni, A. P. C.; Peltzer, P. M.; Attademo, A. M.; Bassó, A.; León, E. J.; Lajmanovich, R. C. Signals from Predators, Injured Conspecifics, and Pesticide Modify the Swimming Behaviour of the Gregarious Tadpole of the Dorbigny’s Toad, Rhinella dorbignyi (Anura: Bufonidae). Can. J. Zool. 2022, 100, 19–27. DOI: 10.1139/cjz-2021-0075.
  • Viran, R.; Unlu, E. F.; Polat, H.; Kocak, O. Investigation of Acute Toxicity of Deltamethrin on Guppies Poecilia reticulata. Ecotoxicol. Environ. Saf. 2003, 55, 82–85. DOI: 10.1016/S0147-6513(02)00096-9.
  • Velísek, J.; Jurcíková, J.; Dobsíková, R.; Svobodová, Z.; Piacková, V.; Máchová, J.; Novotny, L. Effects of Deltamethrin on Rainbow Trout (Oncorhynchus mykiss). Environ. Toxicol. Pharmacol. 2007, 23, 297–301. DOI: 10.1016/j.etap.2006.11.006.
  • Ruiz de Arcaute, C.; Salgado Costa, C.; Demetrio, P. M.; Natale, G. S.; Ronco, A. E. Influence of Existing Site Contamination on Sensitivity of Rhinella dorbignyi (Anura, Bufonidae) Tadpoles to Lorsban 48E Formulation of Chlorpyrifos. Ecotoxicology 2012, 21, 2338–2348.
  • Ceschin, D. G. Toxicogenomics: New Strategies for Ecotoxicology Studies in Autochthonous Species II. The “Omic” Era in Non-Model Species. Transcriptome Analysis for Biomarker Screening. IJENVH 2017, 8, 213. DOI: 10.1504/IJENVH.2017.086180.
  • Suárez, I.; Bodega, G.; Fernández, B. Glutamine Synthetase in Brain: Effect of Ammonia. Neurochem. Int. 2002, 41, 123–142.
  • Geng, Y.; Jiang, L.; Zhang, D.; Liu, B.; Zhang, J.; Cheng, H.; Wang, L.; Peng, Y.; Wang, Y.; Zhao, Y.; et al. Glyphosate, Aminomethylphosphonic Acid, and Glufosinate Ammonium in Agricultural Groundwater and Surface Water in China from 2017 to 2018: Occurrence, Main Drivers, and Environmental Risk Assessment. Sci. Total. Environ. 2021, 769, 144396. DOI: 10.1016/j.scitotenv.2020.144396.
  • Xiong, G.; Deng, Y.; Li, J.; Cao, Z.; Liao, X.; Liu, Y.; Lu, H. Immunotoxicity and Transcriptome Analysis of Zebrafish Embryos in Response to Glufosinate-Ammonium Exposure. Chemosphere 2019, 236, 124423–124411. DOI: 10.1016/j.chemosphere.2019.124423.
  • Ebert, E.; Leist, K. H.; Mayer, D. Summary of Safety Evaluation Toxicity Studies of Glufosinate Ammonium. Food Chem. Toxicol. 1990, 28, 339–349. DOI: 10.1016/0278-6915(90)90108-Y.
  • Lushchak, O. K.; Kubrak, O. I.; Storey, J. M.; Storey, K. B.; Lushchak, V. I. Low Toxic Herbicide Roundup Induces Mild Oxidative Stress in Goldfish Tissues. Chemosphere 2009, 76, 932–937. DOI: 10.1016/j.chemosphere.2009.04.045.
  • Nwani, C. D.; Lakra, W. S.; Nagpure, N. S.; Kumar, R.; Kushwaha, B.; Srivastava, S. K. Mutagenic and Genotoxic Effects of Carbosulfan in Freshwater Fish Channa punctatus (Bloch) Using Micronucleus Assay and Alkaline Single-Cell Gel Electrophoresis. Food Chem. Toxicol. 2010, 48, 202–208. DOI: 10.1016/j.fct.2009.09.041.
  • Shiogiri, N. S.; Paulino, M. G.; Carraschi, S. P.; Baraldi, F. G.; Cruz, C.; Fernandes, M. N. Acute Exposure to Glyphosate-Based Herbicide Affects the Gills and Liver of the Neotropical Fish, Piaractus mesopotamicus. Environ. Toxicol. Pharmacol. 2012, 34, 388–396. DOI: 10.1016/j.etap.2012.05.007.
  • Nwani, C. D.; Ibiam, U. A.; Ibiam, O. U.; Nworie, O.; Onyishi, G.; Atama, C. Investigation on Acute Toxicity and Behavioural Changes in Tilapia zillii Due to Glyphosate Based Herbicide, Force up. J. Anim. Plant. Sci. 2013, 23, 888–892.
  • Cauble, K.; Wagner, R. S. Sublethal Effects of the Herbicide Glyphosate on Amphibian Metamorphosis and Development. Bull. Environ. Contam. Toxicol. 2005, 75, 429–435. DOI: 10.1007/s00128-005-0771-3.
  • Howe, C. M.; Berrill, M.; Pauli, B. D.; Helbing, C. C.; Werry, K.; Veldhoen, N. Toxicity of Glyphosate-Based Pesticides to Four North American Frog Species. Environ. Toxicol. Chem. 2004, 23, 1928–1938. DOI: 10.1897/03-71.
  • Lajmanovich, R. C.; Sandoval, M. T.; Peltzer, P. M. Induction of Mortality and Malformation in Scinax Nasicus Tadpoles Exposed to Glyphosate Formulations. Bull. Environ. Contam. Toxicol. 2003, 70, 612–618.
  • Lajmanovich, R. C.; Attademo, A. M.; Peltzer, P. M.; Junges, C. M.; Cabagna, M. C. Toxicity of Four Herbicide Formulations with Glyphosate on Rhinella arenarum (Anura: Bufonidae) Tadpoles: b-Esterases and Glutathione s-Transferase Inhibitors. Arch. Environ. Contam. Toxicol. 2011, 60, 681–689. DOI: 10.1007/s00244-010-9578-2.
  • Lajmanovich, R. C.; Peltzer, P. M.; Martinuzzi, C. S.; Attademo, A. M.; Basso, A.; Maglianese, M. I.; Colussi, C. L. B-Esterases and Behavioral Biomarkers in Tadpoles Exposed to Pesticide Pyrethroid-TRISADA®. Toxicol. Environ. Health Sci. 2018, 10, 237–244. DOI: 10.1007/s13530-018-0371-3.
  • Lajmanovich, R. C.; Peltzer, P. M.; Martinuzzi, C. S.; Attademo, A. M.; Basso, A.; Colussi, C. L. Insecticide Pyriproxyfen (Dragón®) Damage Biotransformation, Thyroid Hormones, Heart Rate, and Swimming Performance of Odontophrynus americanus Tadpoles. Chemosphere 2019, 220, 714–722. DOI: 10.1016/j.chemosphere.2018.12.181.
  • Attademo, A. M.; Cabagna-Zenklusen, M.; Lajmanovich, R. C.; Peltzer, P. M.; Junges, C.; Bassó, A. B-Esterase Activities and Blood Cell Morphology in the Frog Leptodactylus chaquensis (Amphibia: Leptodactylidae) on Rice Agroecosystems from Santa Fe Province (Argentina). Ecotoxicology 2011, 20, 274–282. DOI: 10.1007/s10646-010-0579-8.
  • Lajmanovich, R. C.; Peltzer, P. M.; Attademo, A. M.; Martinuzzi, C. S.; Simoniello, M. F.; Colussi, C. L.; Cuzziol Boccioni, A. P.; Sigrist, M. First Evaluation of Novel Potential Synergistic Effects of Glyphosate and Arsenic Mixture on Rhinella arenarum (Anura: Bufonidae) Tadpoles. Heliyon 2019, 5, e02601.
  • Lajmanovich, R. C.; Attademo, A. M.; Lener, G.; Cuzziol Boccioni, A. P.; Peltzer, P. M.; Martinuzzi, C. S.; Demonte, L. D.; Repetti, M. R. Glyphosate and Glufosinate Ammonium, Herbicides Commonly Used on Genetically Modified Crops, and Their Interaction with Microplastics: Ecotoxicity in Anuran Tadpoles. Sci. Total Environ. 2022, 804, 150177. DOI: 10.1016/j.scitotenv.2021.150177.
  • Farchi, N.; Soreq, H.; Hochner, B. Chronic Acetylcholinesterase over Expression Induces Multilevelled Aberrations in Mouse Neuromuscular Physiology. J. Physiol. 2003, 546, 165–173. DOI: 10.1113/jphysiol.2002.030841.
  • Lev-Lehman, E.; Evron, T.; Broide, R. S.; Meshorer, E.; Ariel, I.; Seidman, S.; Soreq, H. Synaptogenesis and Myopathy under Acetylcholinesterase over Expression. J. Mol. Neurosci. 2000, 14, 93–105.
  • Richards, S. M.; Kendall, R. J. Physical Effects of Chlorpyrifos on Two Stages of Xenopus laevis. J. Toxicol. Environ. Health A 2003, 66, 75–91. DOI: 10.1080/15287390306461.
  • Barreto, E.; Costa, S.; Demetrio, P.; Lascano, C.; Venturino, A.; Natale, G. S. Sensitivity of Boana pulchella (Anura: Hylidae) Tadpoles to Environmentally Relevant Concentrations of Chlorpyrifos: effects at the Individual and Biochemical Levels. Environ. Toxicol. Chem. 2020, 39, 834–841.
  • Khan, M. Z.; Tabassum, R. Effect of Cypermethrin and Permethrin on Cholinesterase Activity and Protein Contents in Rana tigrina (Amphibia). Environ. Toxicol. 2003, 27, 243–246.
  • Hulbert, A. J.; Else, P. L. Basal Metabolic Rate: History, Composition, Regulation, and Usefulness. Physiol. Biochem. Zool. 2004, 77, 869–876. DOI: 10.1086/422768.
  • Talent, L. G. Effect of Temperature on Toxicity of a Natural Pyrethrin Pesticide to Green Anole Lizards (Anolis carolinensis). Environ. Toxicol. Chem. 2005, 24, 3113–3116. DOI: 10.1897/05-053R.1.
  • Bianchini, A.; Grosell, M.; Gregory, S. M.; Wood, C. M. Acute Silver Toxicity in Aquatic Animals is a Function of Sodium Uptake Rate. Environ. Sci. Technol. 2002, 36, 1763–1766. DOI: 10.1021/es011028t.
  • Grosell, M.; Nielsen, C.; Bianchini, A. Sodium Turnover Rate Determines Sensitivity to Acute Copper and Silver Exposure in Freshwater Animals. Comp. Biochem. Physiol. C 2002, 133, 287–303. DOI: 10.1016/S1532-0456(02)00085-6.
  • Vesela, S.; Vijverberg, AEJ. Effect of Body Size on Toxicity of Zinc in Neonates of Four Differently Sized Effect of Body Size on Toxicity of Zinc in Neonates of Four Differently Sized Daphnia Species. Aquat. Ecol. 2007, 41, 67–73. DOI: 10.1007/s10452-006-9050-6.
  • Cairns, J.; Scheier, A. The Relationship of Bluegill Sunfish Body Size to Tolerance for Some Common Chemicals. Prod. Ind. Waste Conf. Purdue Univ. 1958, 96, 243–252.
  • Pickering, Q. H.; Henderson, C. Acute Toxicity of Some Important Petrochemicals to Fish. J. Water Pollut. Control. Fed. 1966, 38, 1419–1428.
  • Ockleford, C.; Adriaanse, P.; Berny, P.; Brock, T.; Duquesne, S.; Grilli, S.; Hernandez-Jerez, A. F.; Hougaard Bennekou, S.; Klein, M.; Kuhl, T.; et al. Scientific Opinion on the State of the Science on Pesticide Risk Assessment for Amphibians and Reptiles. EFSA J. 2018, 16, 5125.
  • Ultsch, G. R.; Bradford, D. F.; Freda, J. Physiology: Coping with the Environment. In McDiarmid, R. W.; Altig, R.; Eds.; Tadpoles: The Biology of Anuran Larvae. University of Chicago Press: Chicago, 1999; pp 189–214.
  • Bielby, J.; Cunningham, A. A.; Purvis, A. Taxonomic Selectivity in Amphibians: Ignorance, Geography or Biology? Anim. Conserv. 2006, 9, 135–143. DOI: 10.1111/j.1469-1795.2005.00013.x.
  • Vaira, M.; Pereyra, L. C.; Akmentins, M. S.; Bielby, J. Conservation Status of Amphibians of Argentina: An Update and Evaluation of National Assessments. Amphibian Reptile Conserv. 2017, 11, [General Section]: 36–44. (e135).

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